Association between Cardiometabolic Profile and Dietary Characteristics among Adults with Type 1 Diabetes Mellitus

RESEARCH

Original Research

Association between Cardiometabolic Profile and Dietary Characteristics among Adults with Type 1 Diabetes Mellitus Véronique Gingras, MSc, RD*; Catherine Leroux, RD*; Katherine Desjardins, MSc, RD*; Valérie Savard, RD*; Simone Lemieux, PhD, RD*; Rémi Rabasa-Lhoret, MD, PhD; Irene Strychar, PhD, RD* ARTICLE INFORMATION Article history: Submitted 13 May 2014 Accepted 10 April 2015 Available online 4 June 2015

Keywords: Type 1 diabetes mellitus Nutrition guidelines Diet Mediterranean Cardiometabolic risk 2212-2672/Copyright ª 2015 by the Academy of Nutrition and Dietetics. http://dx.doi.org/10.1016/j.jand.2015.04.012 *

Certified in Canada.

ABSTRACT Background The Mediterranean-style dietary pattern has been associated with several cardiometabolic benefits, yet no study has assessed the potential benefits of this diet in adults with type 1 diabetes mellitus (T1DM). Objective The objective of the present study was to examine the association between cardiometabolic profile and alignment of the diet with 1) Canadian nutrient recommendations for T1DM in terms of fat, protein, carbohydrate, saturated fat, dietary fiber, and sodium and 2) a Mediterranean-style dietary pattern among adults with T1DM. Design/participants/setting This is a cross-sectional analysis including 118 adults with T1DM recruited between 2011 and 2013 in Montreal, Canada. Statistical analyses Body mass index (calculated as kg/m2), waist circumference, truncal fat percentage (dual-energy x-ray absorptiometry), blood pressure, and lipid profile values were measured. Insulin sensitivity was estimated (estimated glucose disposal rate). A 3-day food record was completed and physical activity was measured with a motion sensor. Differences for the cardiometabolic profile between groups with a diet meeting the Canadian nutrient recommendations for T1DM (percentage of energy from fat, protein, carbohydrate, saturated fat, as well as grams of dietary fiber and milligrams of sodium) or not were examined with general linear models. A Mediterranean diet score was calculated (range¼0 to 44) and Pearson correlations between this score and cardiometabolic variables were computed. Significance was set at P0.05. Results Participants’ meanstandard deviation age was 44.312.3 years, glycated hemoglobin was 8.0%1.1%, and Mediterranean diet score was 20.25.0. Having a diet that meets at least three nutritional recommendations was associated with a lower truncal fat percentage (28.0% vs 32.2%; P¼0.01) only. In contrast, the Mediterranean diet score was inversely correlated with body mass index (r¼0.30, P¼0.002), waist circumference (r¼0.31, P¼0.002), truncal fat percentage (r¼0.38, P<0.001), systolic (r¼0.20, P¼0.03) and diastolic blood pressure (r¼0.23, P¼0.01), and was directly correlated with estimated glucose disposal rate (r¼0.22, P¼0.03), after adjustments for energy intake, sex, and age. The association with estimated glucose disposal rate was no longer significant (P¼0.055) after adjustment for physical activity level. Conclusions These results suggest that a higher Mediterranean diet score in the context of T1DM is associated with a favorable cardiometabolic profile. Further research is needed to confirm these findings. J Acad Nutr Diet. 2015;115:1965-1974.

T

HE NUTRITIONAL RECOMMENDATIONS FOR INdividuals with type 1 diabetes mellitus (T1DM)1 are similar to those for the general population. 2 The 2013 Canadian Diabetes Association’s nutritional recommendations for individuals with T1DM focus on macronutrients and state that individuals should eat a balanced diet with 45% to 60% of daily energy intake (DEI) from carbohydrate (CHO), 15% to 20% from protein (PRO), and 20% to 35% from total dietary fat, with saturated fat intake limited to 7% of the DEI.1 In addition, high intake of dietary fiber (25 to 50 g/day),1 as well as low intake of sodium (<2,300 mg/ ª 2015 by the Academy of Nutrition and Dietetics.

day)3 are also recommended. For individuals with type 2 diabetes mellitus (T2DM), specific dietary patterns (eg, the Mediterranean-style dietary pattern or the Dietary Approaches to Stop Hypertension diet) are also recommended, but these dietary patterns are not included in recommendations for T1DM.1 In the American Diabetes Association’s guidelines, as well as in the Academy of Nutrition and Dietetics Evidence-Based Nutrition Practice Guidelines for adults with T1DM and T2DM, it is mentioned that a variety of eating patterns are acceptable for the management of diabetes and a specific dietary pattern should be recommended according to JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS

1965

RESEARCH personal preferences and metabolic goals.4,5 Finally, the European Association for the Study of Diabetes’ guidelines suggest that several dietary patterns are acceptable, including a Mediterranean-style dietary pattern with a higher intake of fat.6 The Mediterranean-style dietary pattern is not a unique dietary pattern and varies from one region to another according to food availability and preferences. The Mediterranean-style dietary pattern is characterized by abundant plant-based foods, such as vegetables, fruits, whole grains, beans and legumes, nuts, and seeds. Olive oil is typically the principal source of fat. Dairy products such as cheese and low-fat yogurt, as well as fish, poultry, and eggs are consumed in low to moderate amounts, and red meat is consumed in small amounts. The Mediterranean-style dietary pattern is low in saturated fat (7% to 8%) and total dietary fat ranges from 25% to 35% of DEI.7 Alignment of the diet with a Mediterranean-style dietary pattern can be measured with a derived score and numerous different types of scores have been used to examine associations between the Mediterranean-style dietary pattern, as an integral entity, and a variety of health outcomes.8 One method uses the Mediterranean-style dietary pattern pyramid as a reference with pre-established scores being attributed to the elements of the pyramid. Higher scores are attributed to the elements at the base of the pyramid (grain products, vegetables, legumes/nuts/seeds, fruits, olive oil, dairy products, and fish) and, inversely, a lower score is attributed for the elements at the top of the pyramid (eggs, sweets, and red meat). This method has been used in studies conducted among a North American population.9-11 In the present decade, the health benefits associated with the adoption of a Mediterranean-style dietary pattern have been studied extensively in diverse populations, such as individuals with T2DM or normal-weight and overweight or obese adults without diabetes. The adoption of a Mediterranean-style dietary pattern has a favorable impact on cardiovascular risk and studies have shown beneficial effects of this diet on lipid profile, blood pressure, insulin sensitivity, and body composition.12,13 Only one study has examined the impact of a Mediterranean-style dietary pattern intervention among children and adolescents with T1DM. Cadario and colleagues14 found an improvement in the lipid profile (decreased low-density lipoprotein [LDL] cholesterol, nonhigh-density [HDL] lipoprotein cholesterol, and total cholesterol to high-density lipoprotein cholesterol ratios) and the dietary intake (decreased total dietary fats and cholesterol; increased fiber consumption) of children and adolescents with T1DM (n¼96) who underwent three nutritional counseling sessions designed to increase adherence to a Mediterranean-style dietary pattern, without caloric restriction. Despite the well-known benefits associated with the Mediterranean-style dietary pattern, no study has assessed the potential benefits of this diet in adults with T1DM, a population at high risk for cardiovascular disease.15 The objective of the present study was to examine the association between cardiometabolic profile and alignment of the diet with 1) Canadian nutrient recommendations for T1DM and 2) a Mediterranean-style dietary pattern among adults with T1DM. The principal hypothesis was that participants whose dietary profile is closer to a Mediterraneanstyle dietary profile will present a more favorable 1966

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cardiometabolic profile than participants whose dietary profile does not reflect a Mediterranean-style dietary pattern. The secondary hypothesis was that alignment of the diet with a greater number of nutrient recommendations for T1DM will be beneficially associated with the cardiometabolic profile of participants.

METHODS Study Population This is a secondary analysis of a cross-sectional observational study that included 124 adults with T1DM recruited at the Institut de Recherches Cliniques de Montréal and at the Montreal University Hospital Centre between 2011 and 2013.16 Patients aged 18 years, with T1DM duration 6 months and treated with multiple daily injections or continuous subcutaneous insulin infusion using rapid and basal insulin analogs were invited to participate. Exclusion criteria included one severe hypoglycemic episode (requiring assistance) during the previous 3 months or 3 severe episodes in the previous year and pregnancy. All subjects gave their written consent before data collection and ethical approval was obtained from the Institut de Recherches Cliniques de Montréal and the Montreal University Hospital Centre ethic review boards.

Data Collection Data were collected using standardized procedures. Participants came to the clinic at Institut de Recherches Cliniques de Montréal for two visits, approximately 1 week apart. At visit 1, weight, height, waist circumference, and blood pressure were measured. Weight was measured in light clothing and without shoes to the nearest 0.1 kg on a calibrated balance, height was measured to the nearest millimeter with a stadiometer, and body mass index (BMI) was then calculated (kg/m2). Waist circumference was measured to the nearest 0.1 cm at the top of the iliac crest in standing subjects.17 Blood pressure was measured three times using an automatic sphygmomanometer after a 5-minute rest period and mean values were calculated. A motion sensor (SenseWear Pro 3 Armband; HealthWear Bodymedia) was placed for 3 days to measure physical activity and a food record was given to collect concomitant nutritional data. Participants were instructed by a registered dietitian (RD*) on how to use the device according to manufacturer’s instructions and how to complete the 3-day food record. They were instructed to measure all food and beverages consumed (in mL) and provided food weights (g), if available (food scales were not provided to participants). They were also asked to maintain their usual lifestyle habits. At visit 2, a fasting blood sample was drawn to measure glycated hemoglobin (A1c) and blood lipids (total, LDL, and HDL cholesterol, and triglycerides). Truncal fat percentage was determined from an iDXA (dual x-ray absorptiometry) scan using a LUNAR Prodigy system (version 6.10.019; General Electric Lunar Corporation). Data on sociodemographic status were collected with a self-administered questionnaire. Participants also brought back the motion sensor and an RD

*Certified in Canada; the equivalent of “registered dietitian nutritionist.” December 2015 Volume 115 Number 12

RESEARCH reviewed the food record with them. Data from the motion sensor were analyzed using Innerview Research software (version 6.1, 2007, HealthWear Bodymedia). Physical activity level (PAL) was calculated by dividing total energy expenditure by the estimated resting energy expenditure, two measures obtained from the motion sensor.18 A PAL 1.7 corresponds to the recommended threshold defining an active lifestyle.19 An endocrinologist recorded medical history, diabetes-related complications, and use of antihypertensive and lipid-lowering medication. The medical visit was conducted at either visit 1 or visit 2, depending on the availability of the physician. Insulin resistance was estimated from the estimated glucose disposal rate formula, a method validated by Williams and colleagues20 with the euglycemic hyperinsulinemic clamp: (24.31[12.22waist-to-hip ratio] [3.29hypertension][0.57A1c]). In this formula, hypertension corresponds to a blood pressure >140/90 mm Hg or use of antihypertensive medication. A higher estimated glucose disposal rate value corresponds to greater insulin sensitivity.

Nutritional Scoring The food records were analyzed by an RD using the Food Processor SQL (version 10.8, 2011, ESHA Research) with the 2007 Canadian Nutrient File and, if necessary, food label information was added to the database. A second RD verified all the food record entry. Mean daily dietary intakes for CHO, PRO, total dietary fat, saturated fat, dietary fiber, and sodium were computed to allow comparisons with the percentage of DEI recommended for each nutrient and participants were considered as having a diet in alignment with the Canadian nutrient recommendations for T1DM when they met three or more of six recommendations. A Mediterranean-style dietary score from Goulet and colleagues21 and based on the Mediterranean pyramid components (ie, grains, fruits, vegetables, legumes/nuts/seeds, olive oil, dairy products, fish, poultry, eggs, sweets, and red meat/processed meat) was then derived from the 3-day food records (Table 1). Subscores for each component were calculated (from 0 to 4). A high score was attributed for a high consumption of the elements at the base of the pyramid and, inversely, a lower frequency of intake for the elements at the top of the pyramid was associated with a higher score. The score ranges on a scale of 0 to 44 points; a higher score denoting a better alignment of the diet with a Mediterranean-style dietary pattern.

Table 1. Components of the Mediterranean diet score (total score from 0 to 44)21

Dietary components

Criteria for minimal score (0)

Criteria for maximal score (4)

ƒƒƒƒƒportions/dƒƒƒƒƒ! Whole-grain products

<1

7

Vegetables

<1

4

Fruits

<1

4

Legumes, nuts, and seed

<0.5

>2

Olive oil, olives, and margarine made of olive oil

<1

4

Milk and dairy products

<1 or >4

2e3

Fish and seafood

Never

3

Poultry (other than breaded)

Never

3

Eggs

7

0e4

Sweets

7

<1

Red meat/processed meat

7

<1

ƒƒƒƒportions/wkƒƒƒƒ!

the Mediterranean diet score were adjusted for energy intake, sex, and age (Table 4). Exploratory analyses were conducted with adjustment for PAL and are discussed in the Results section (data not shown). Pearson partial correlations between the Mediterranean diet score and the anthropometric measurements (BMI, waist circumference, and truncal fat percentage) and the metabolic measurements (lipid profile, A1c, estimated insulin sensitivity, and blood pressure) were computed for all participants and adjusted for energy intake, age, and sex (Table 5). All analyses with lipid profile variables were also adjusted for lipid-lowering medication use and all analyses with blood pressure were also adjusted for antihypertension medication use. All study variables were examined for normality of distribution before analysis and skewed variables were log-10 transformed. All statistical analyses were performed using the Statistical Package for Social Sciences 20.0 (SPSS, Inc, 2013) and statistical significance was defined as P0.05.

Statistical Analyses Descriptive statistics (mean and standard deviation [SD] for continuous variables or percentage for categorical variables) were computed for the dietary profile (Table 2). Differences between participants according to alignment of their diet with Canadian nutrient recommendations for T1DM (CHO, PRO, total dietary fat, saturated fat, dietary fiber, and sodium1) were examined with general linear models adjusted for age, sex, and energy intake (Table 3). Differences for the dietary, anthropometric, and metabolic profiles between groups who met the nutrient recommendations (three or more of six) or not (two or less of six), as well as groups with a lower (score below the median [<19]) or higher (score above the median [19]) Mediterranean diet score were examined with general linear models and associations with December 2015 Volume 115 Number 12

RESULTS Of the 124 participants recruited, 6 were excluded because of incomplete 3-day food records (missing days or incomplete information, eg, missing weight of food consumed). MeanSD age of the participants (n¼118) of the present study was 44.312.3 years, with a diagnosis of T1DM since 23.112.6 years. Mean A1c was 8.0%1.1% and most individuals were treated with multiple daily injections (68%) rather than continuous subcutaneous insulin infusion (32%). A high proportion of participants used antihypertensive (36.4%) and lipid-lowering (45.8%) medication. Participants were mostly white (94%), physically inactive (mean PAL 1.50.3; 70% of participants with a PAL <1.7), living with a JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS

1967

RESEARCH Table 2. Dietary characteristics of adults with type 1 diabetes mellitus in an observational study conducted in Montreal, Canada (n¼118) Meets the Canadian Nutrient Recommendationsa for T1DMb Dietary characteristics

Overall (n[118)

Men (n[57)

Women (n[61)

Energy, kcal/d

2,172535

2,463474

1,899438

<0.001

P valuec

ƒƒƒƒƒmeanstandard deviationƒƒƒƒƒ! Carbohydrate, % of DEI

d

Overall (n[118)

Men (n[57)

Women (n[61)

P valuec

ƒƒƒƒƒƒƒƒƒ%ƒƒƒƒƒƒƒƒƒ! —

—

—

—

45.37.4

45.06.8

45.77.9

0.60

51.7

49.1

54.1

0.71

17.23.9

16.92.7

17.54.8

0.42

52.5

57.9

47.5

0.28

Total fat, % of DEI

35.07.0

35.27.3

34.86.7

0.73

45.4

47.5

43.9

0.69

Saturated fat, % of DEI

11.23.0

11.63.0

10.83.0

0.14

7.6

5.3

9.8

0.49

Protein, % of DEI

Dietary fiber, g/d Sodium, mg/d Mediterranean diet scoree

22.47.8

22.98.3

21.87.3

0.44

33.1

35.0

31.1

0.70

2,9451,190

3,4011,172

2,5191,046

<0.001

33.1

15.8

49.2

<0.001

20.25.0

19.44.1

21.05.7

0.08

—

—

—

—

Canadian nutrient recommendations for T1DM: carbohydrate 45% to 60% of DEI, protein 15% to 20% of DEI, total fat <35% of DEI, saturated fat 7% of DEI, dietary fiber 25 to 50 g/d, and sodium <2,300 mg/d. b T1DM¼type 1 diabetes mellitus. c P value for the difference between men and women. d DEI¼daily energy intake. e The Mediterranean diet score ranges on a scale of 0 to 44 points; a higher score denoting a better alignment of the diet with a Mediterranean-type dietary pattern. a

partner (66%), had a post-secondary degree (76%), and a family income >50,000 CAN$/year (>46,305 US$/year) (69%). The dietary intakes of the participants are presented in Table 2. MeanSD energy intake was 2,172535 kcal/day (men 2,463474 kcal/day; women 1,899438 kcal/day; P<0.001). About half of the participants met the Canadian Diabetes Association’s nutritional recommendations for T1DM for PRO (15% to 20% of DEI), total dietary fat (20% to 35% of DEI), and CHO (45% to 60% of DEI), and approximately one-third of the participants met the recommendations for dietary fiber (25 to 50 g/day) and sodium intake (<2,300 mg/day; 16% for men vs 49% for women; P<0.001). Eight percent of participants met the recommendations for saturated fat (<7% of DEI). Beside the differences in energy and sodium intakes, there was no significant difference between men in women in the intake of any nutrient expressed as percentage of DEI. As for the number of nutritional recommendations met, 55% of participants met two or less of the recommendations, and 45% of the participants met three or more of the recommendations (data not shown). Finally, participants had a mean Mediterranean diet score of 20.25.0, with no significant difference between men and women (P¼0.08). The scores for each Mediterranean-style dietary pattern component were also examined (data not shown). The components with the highest scores, on a scale of 0 to 4, were vegetables (3.11.1), milk and dairy products (3.11.3), and eggs (3.11.4). Components with the lowest scores were olive oil, olives, and margarine from olive oil (0.20.5), red meat/processed meat (1.01.3), and legumes, nuts, and seeds (1.11.2). For whole-grain products, fruits, fish and seafood, poultry and sweets, the components’ scores ranged from 1.5 to 2.2. The anthropometric and metabolic profiles of participants according to the alignment of their diet to Canadian nutrient 1968

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recommendations for T1DM are presented in Table 3. Participants who met the recommended dietary intake for CHO (45% to 60% of DEI) had a lower truncal fat percentage (P¼0.03) and A1c (P¼0.03) and higher estimated glucose disposal rate (P¼0.04) compared with participants who did not meet the recommendation. No difference in anthropometric and metabolic variables was found between participants who met the recommendation or not for dietary fiber, total dietary fat, and saturated fat. Participants who met the recommendation for PRO (15% to 20% of the DEI) had a lower systolic blood pressure (P¼0.03) than participants who did not. Finally, participants who met the recommendation for sodium (<2,300 mg/day) had a higher total cholesterol (P¼0.004) and a higher LDL cholesterol (P¼0.002). The differences observed between participants who met the recommended dietary intake for CHO or not were no longer significant after further adjustment for PAL (data not shown). Dietary, anthropometric, and metabolic profiles of participants according to alignment of their diet with nutrient recommendations for T1DM and a Mediterranean-style dietary pattern are outlined in Table 4. Participants who met three or more recommendations had higher intakes of CHO and dietary fiber (P<0.001) and lower intakes of total dietary fat , saturated fat (P<0.001), and sodium (P¼0.01). Participants who met three or more of the six recommendations had a lower truncal fat percentage (P¼0.01) compared with those who met less than three recommendations; however, no other differences in anthropometric or metabolic variables were found. The association between participants with either a lower (<19) or higher (19) Mediterranean diet score and their dietary, anthropometric, and metabolic profiles was examined. Participants with a higher Mediterranean diet score had higher CHO (P¼0.05) and dietary fiber intake (P<0.001), as well as December 2015 Volume 115 Number 12

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Table 3. Anthropometric and metabolic characteristicsa of Canadian adults with type 1 diabetes mellitus according to alignment of their diet with Canadian nutrient recommendations for type 1 diabetes mellitus (n¼118b) Carbohydrate (45% to 60% of DEIc) Anthropometric and metabolic variables

No (n[57)

Yes (n[61)

Dietary Fiber (25 to 50 g/d) No (n[79)

Yes (n[39)

Protein Total Fat (15% to 20% of DEI) (20% to 35% of DEI) No (n[56)

Yes (n[62)

No (n[64)

Yes (n[54)

Saturated Fat (<7% of DEI) No (n[109)

Yes (n[9)

Sodium (<2,300 mg/d) No (n[79)

Yes (n[39)

ƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒmeanstandard deviationƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒƒ! Anthropometric variables Body mass indexd

26.64.3

Waist circumference, cm

90.912.3 87.512.7

89.413.2 88.711.5 88.712.6 89.612.7 90.013.3 88.211.8 89.512.5 84.613.2 89.612.1 88.313.7

Truncal fat, %

32.39.9

28.19.9*

31.210.1 28.410.0 30.510.4 30.09.9

8.21.1

7.81.0*

25.44.6

25.84.6

26.34.4

25.94.7

26.14.4

26.44.8

25.64.1

26.24.5

31.510.0 28.710.1 30.39.7

24.14.2

26.24.4

28.914.1 29.79.7

25.74.7 31.210.7

Metabolic variables Glycated hemoglobin, % Total cholesterol, mg/dL

e

8.11.0

7.91.2

8.01.0

8.01.0

8.01.1

7.91.0

8.01.1

8.31.0

8.01.1

7.91.1

16530

16732

16632

17036

16429

16829

16636

16733

16315

16130

18034**

8830

8724

8727

8827

9030

8624

8824

8630

8927

7416

8424

9431**

HDLg cholesterol, mg/dLe

6418

6314

6517

6114

6518

6315

6317

6416

6315

7520

6115

7016

Triglycerides, mg/dL

h

8146

7530

7635

8346

7941

7937

8144

7431

7940

7622

7943

7728

Systolic blood pressure, mm Hg

11512

11414

11615

11310

11715

11312*

11510

11416

11513

11413

11512

11615

Diastolic blood pressure, mm Hg

728

709

719

697

719

708

728

699

719

674

719

708

7.72.4

7.92.5

Estimated glucose disposal rate, mg/kg/min

7.212.51 8.292.30* 7.592.54 8.122.27 7.762.63 7.772.31 7.612.48 7.932.43 7.842.44 6.862.54

a

Comparisons were examined with general linear model and analyses were adjusted for age, energy, and sex. Analyses for blood pressure were additionally adjusted for antihypertensive medication use and analyses for lipid profile were additionally adjusted for lipid-lowering medication use. The differences observed between participants who met the recommended dietary intake for carbohydrate or not were no longer significant after further adjustment for physical activity level. b Data are missing for truncal fat, total cholesterol, and triglycerides (n¼5), for LDL and HDL cholesterol (n¼6), for systolic and diastolic blood pressure (n¼2), and for estimated glucose disposal rate (n¼1). c DEI¼daily energy intake. d Calculated as kg/m2. e To convert mg/dL cholesterol to mmol/L, multiply mg/dL by 0.0259. To convert mmol/L cholesterol to mg/dL, multiply mmol/L by 38.6698. Total cholesterol of 150 mg/dL¼3.88 mmol/L. f LDL¼low-density lipoprotein. g HDL¼high-density lipoprotein. h To convert mg/dL triglycerides to mmol/L, multiply mg/dL by 0.0113. To convert mmol/L triglycerides to mg/dL, multiply mmol/L by 88.574. Triglycerides of 75 mg/dL¼0.85 mmol/L. *P<0.05. **P<0.01.

1969

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16835

LDLf cholesterol, mg/dLe

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Alignment of the Diet with Canadian Nutrient Recommendations for T1DM Lower (£2/6) (n[65)

Higher (‡3/6) (n[53)

P value

ƒƒƒƒ meanstandard deviationƒƒƒƒ!

Alignment of the Diet with a MediterraneanType Dietary Pattern Lower (score <19) (n[58)

Higher (score ‡19) (n[60)

P value

ƒƒƒƒƒƒƒƒmeanstandard deviationƒƒƒƒƒƒƒƒ!

Dietary variables Energy, kcal/d

2,185467

2,156613

0.23

2,218609

2,126453

0.36

Carbohydrate, % of DEIc

438

495

<0.001

417

448

0.05

Protein, % of DEI

174

174

0.95

185

173

0.12

Total fat, % of DEI

387

325

<0.001

367

346

0.09

123

102

<0.001

123

103

19.15.3

26.38.6

<0.001

19.57.7

25.26.9

<0.001

3,1321,110

2,7151,252

0.01

3,2221,420

2,677840

0.01

Body mass indexd

26.34.7

25.64.2

0.33

26.94.5

25.14.3

0.02

Waist circumference, cm

89.612.9

88.612.4

0.17

92.313.2

86.111.3

<0.001

Truncal fat, %

32.29.5

28.010.3

0.01

32.09.9

28.410.0

0.002

8.11.1

7.81.0

0.06

8.11.0

7.91.1

0.29

Saturated fat, % of DEI Dietary fiber, g/d Sodium, mg/d

0.003

Anthropometric variables

Metabolic variables Glycated hemoglobin, % e

Total cholesterol, mg/dL

16733

16631

0.96

16829

16536

0.50

LDLf cholesterol, mg/dLe

8926

8627

0.79

9024

8530

0.53

HDLg cholesterol, mg/dLe

6317

6515

0.57

6217

6516

0.72

h

8043

7632

0.74

8548

7327

0.19

Systolic blood pressure, mm Hg

11512

11415

0.61

11814

11212

0.02

Diastolic blood pressure, mm Hg

729

698

0.11

728

698

0.05

7.582.58

7.992.30

0.21

7.172.65

8.332.12

0.008

Triglycerides, mg/dL December 2015 Volume 115 Number 12

Estimated glucose disposal rate, mg/kg/min a

Comparisons were examined with general linear model and analyses for the anthropometric and metabolic variables were adjusted for age, energy, and sex. Analyses for blood pressure were additionally adjusted for antihypertensive medication use and analyses for lipid profile were additionally adjusted for lipid-lowering medication use. All differences observed remained significant after further adjustment for physical activity level except for the association between alignment with the Mediterranean-type dietary pattern and body mass index. b Data are missing for truncal fat, total cholesterol, and triglycerides (n¼5), for LDL and HDL cholesterol (n¼6), for systolic and diastolic blood pressure (n¼2) and for estimated glucose disposal rate (n¼1). c DEI¼daily energy intake. d Calculated as kg/m2. e To convert mg/dL cholesterol to mmol/L, multiply mg/dL by 0.0259. To convert mmol/L cholesterol to mg/dL, multiply mmol/L by 38.6698. Total cholesterol of 150 mg/dL¼3.88 mmol/L. f LDL¼low-density lipoprotein. g HDL¼high-density lipoprotein. h To convert mg/dL triglycerides to mmol/L, multiply mg/dL by 0.0113. To convert mmol/L triglycerides to mg/dL, multiply mmol/L by 88.574. Triglycerides of 75 mg/dL¼0.85 mmol/L.

RESEARCH

1970

Table 4. Dietary, anthropometric and metabolic characteristics of Canadian adults with type 1 diabetes mellitus according to alignment of their diet with Canadian nutrient recommendations for type 1 diabetes mellitus and Mediterranean-type dietary patterna (n¼118b)

RESEARCH Table 5. Adjusted Pearson correlationa between the Mediterranean diet score and anthropometric and metabolic parameters in Canadian adults with type 1 diabetes mellitus (n¼118b) Anthropometric and metabolic parameters

r

Body mass indexc

0.30

Waist circumference, cm

0.31

0.002

Truncal fat, %

0.38

<0.001

Glycated hemoglobin, %

0.12

0.25

Total cholesterol, mg/dL

0.07

0.48

P value 0.002

LDL cholesterol, mg/dL

0.08

0.41

HDLe cholesterol, mg/dL

0.07

0.47

Triglycerides, mg/dL

0.16

0.09

Systolic blood pressure, mm Hg

0.20

0.03

Diastolic blood pressure, mm Hg

0.23

0.01

0.23

0.02

d

Estimated glucose disposal rate, mg/kg/min

a Correlations are adjusted for age, energy, and sex. Correlations with lipid profile variables are additionally adjusted for lipid-lowering medication use and correlations with blood pressure are additionally adjusted for antihypertensive medication use. Further adjustment for physical activity level did not alter correlations except for the association with estimated glucose disposal rate, which was no longer significant (P¼0.055). b Data are missing for truncal fat, total cholesterol, and triglycerides (n¼5), for LDL and HDL cholesterol (n¼6), for systolic and diastolic blood pressure (n¼2) and for estimated glucose disposal rate (n¼1). c Calculated as kg/m2. d LDL¼low-density lipoprotein. e HDL¼high-density lipoprotein.

lower saturated fat (P¼0.003) and sodium intakes (P¼0.01). Participants with a higher Mediterranean diet score also had lower BMI (P¼0.02), waist circumference (P<0.001), truncal fat percentage (P¼0.002), systolic blood pressure (P¼0.02), diastolic blood pressure (P¼0.05), and they had higher estimated glucose disposal rate (P¼0.008). All differences observed remained significant after adjustment for PAL, except for the association between alignment with the Mediterranean-style dietary pattern and BMI (data not shown). Finally, energy-, age-, and sex-adjusted Pearson correlations were performed to examine the association between the Mediterranean diet score and variables from the metabolic and anthropometric profile in the participants (Table 5). The Mediterranean diet score was inversely correlated with BMI (r¼0.30, P¼0.002), waist circumference (r¼0.31, P¼0.002), truncal fat percentage (r¼0.38, P<0.001), systolic (r¼0.20, P¼0.03), and diastolic (r¼0.23, P¼0.01) blood pressure, and was directly correlated with estimated glucose disposal rate (r¼0.23, P¼0.02). The associations with lipid profile variables were also adjusted for lipid-lowering medication use and the associations with blood pressure were also adjusted for antihypertension medication use. No difference was observed for A1c or the lipid profile. Further adjustment for PAL did not alter correlations except for the association with estimated glucose disposal rate, which was no longer significant (P¼0.055). December 2015 Volume 115 Number 12

DISCUSSION The proportion of participants meeting the Canadian nutritional recommendations for T1DM was low in the present study. Only one-third or less of the participants met the recommended nutritional targets, with the exception of CHO, PRO, and total dietary fat, for which approximately 50% of participants met the recommendation. Also, one-third of participants met only one or none of the nutrient recommendations. A diet meeting nutrient recommendations, mainly CHO, was associated with a favorable anthropometric profile (truncal fat) and some favorable aspects of the metabolic profile. The alignment of the diet with a Mediterranean-style dietary pattern was associated with favorable anthropometric (BMI, waist circumference, and truncal fat) and metabolic (diastolic blood pressure and insulin sensitivity) profiles. However, after adjustment for PAL, the associations with CHO, as well as the association between Mediterranean-style dietary pattern and BMI, were no longer significant. Several associations of the present study were attenuated or no longer significant after adjustment for PAL, which could be explained by the strong association between physical activity and cardiometabolic profile, as demonstrated in previous studies in adults with T1DM.22,23 Results of the present study on alignment of the diet with nutritional recommendations are consistent with other observational studies, which also suggested that the diets of individuals with T1DM frequently do not meet nutritional recommendations. A study conducted by Snell-Bergeon and colleagues24 showed that patients had higher intakes than recommended for total dietary fat and saturated fat and lower intakes of CHO. Only the recommendation for PRO was met by most patients. They also showed for total dietary fat, saturated fat, and CHO, that alignment with recommendations was significantly lower among patients with T1DM compared with patients without diabetes. Other cohort studies conducted among patients with T1DM have also shown that saturated fat intakes are considerably higher than recommended and fiber intakes are lower than recommended.25,26 These discrepancies between dietary intakes and nutritional recommendations are also present in the general population. Results from the Canadian Community Health Survey conducted in 2004 showed that one-quarter of adults aged 19 years and older exceeded 35% of their DEI as total dietary fat.27 In this survey, adults, on average, consumed 31.3% of their energy as total dietary fat, 16.5% as PRO, and 49.1% as CHO. Alignment of the diet with a Mediterranean-style diet was also relatively low in the present study, with a mean score of 20.25.0 (men: 19.44.1 and women: 21.05.7; P¼0.08). This mean score is similar to the one observed in a study conducted among healthy women from another Quebec francophone urban area (21.33.5).9 The low Mediterranean diet score observed in our study is mostly explained by low scores for olive oil/olives/margarine made of olive oil, red/ processed meat, and legumes/nuts/seed consumption. Although a Mediterranean-style dietary pattern is not the typical dietary pattern observed in this study’s geographical region, it appears feasible to promote a Mediterranean-style dietary pattern in a non-Mediterranean population (ie, a population from the province of Québec) in uncontrolled free-living conditions as shown by Goulet and colleagues21 JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS

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RESEARCH after a 12-week nutritional intervention including group and individual sessions with an RD. Participants with a diet in alignment with nutrient recommendations and in alignment with a Mediterranean-style dietary pattern had higher intakes of both CHO and dietary fiber, with lower intakes of saturated fat and sodium. However, only patients who met three or more of six recommendations had lower intakes of total dietary fat. This lower total dietary fat intake might explain why alignment of diet with nutrient recommendations was associated with only a few cardiometabolic benefits. A weight-loss study conducted among moderately obese men and women showed significantly higher weight loss, reduction of insulin levels, and improvement in glycemic control in patients prescribed a Mediterranean diet rather than a low-fat diet.28 In the general population, in individuals with T2DM as well as in overweight/obese patients, the benefits of the Mediterranean-style dietary pattern on the cardiometabolic profile have been well established. Several studies have shown benefits of this diet for weight loss,28,29 on insulin resistance,30 dyslipidemia,31 blood pressure,32 endothelial function,30,33 and inflammation11,30,34,35 and even recently on the primary prevention of cardiovascular diseases.36 In adults with T1DM, the impact of a Mediterranean-style dietary pattern has not been studied yet. The only study that has examined the impact of a Mediterranean-style dietary pattern intervention among youth with T1DM found an improvement in the lipid profile (decreased LDL cholesterol, non-HDL cholesterol, and total cholesterol to HDL cholesterol ratios) and the nutritional intake (decreased total dietary fat and cholesterol; increased fiber consumption).14 Their results did not show any improvement in A1c levels and showed a minor increase in BMI (0.3) and an increase in daily insulin units (5.1 units) in the whole group at 6 months. In the present study, no association was found between a higher Mediterranean diet score and the lipid profile of adults with T1DM. This lack of association could be partially explained by the high rates of lipid-lowering medication in our present sample (45.8%). One study has also investigated the effects of adherence to a Dietary Approaches to Stop Hypertension diet in youth with T1DM (617 patients <20 years old).37 They showed overall poor adherence with low variability over time and, as the Dietary Approaches to Stop Hypertension diet score increased, A1c decreased.37 To our knowledge, no other study has assessed the benefits of educating patients with T1DM regarding specific dietary patterns. The evidence for nutritional recommendations is needed, especially considering the evolving cardiometabolic profile of these patients. Overweight/obesity38-40 and increased cardiometabolic risk40-43 are growing concerns among patients with T1DM. Lifestyle may play an important role in the prevention of these complications,44 and appropriate nutritional strategies need to be implemented. Despite the limitations related to the cross-sectional design of the present study, our data suggest that some benefits may be associated with a diet in alignment with a Mediterranean-style dietary pattern in adults with T1DM. The main strength of the present study is the detailed characterization of the diet, as all participants completed a food record over 3 days for dietary assessment.45 Also, a qualitative assessment of the dietary profile (ie, the Mediterranean diet score) was included. This study is the first to 1972

JOURNAL OF THE ACADEMY OF NUTRITION AND DIETETICS

assess the alignment of the diet with a Mediterranean diet profile in adult patients with T1DM. The present study also has limitations. The first limitation is the characteristics of the study sample. The present sample is rather small and homogenous with most participants being white with a relatively high socioeconomic status (high family income and post-secondary degree); comparison between the alignment of the diet with dietary guidelines according to socioeconomic status or ethnicity was not possible. Also, the participants assessed were adults with well-controlled T1DM. In addition, our cross-sectional design does not allow establishing a causal relationship between the Mediterraneanstyle dietary pattern and a favorable cardiometabolic profile. However, the benefits observed in the present cohort study support the need for intervention studies targeting diet quality in patients with T1DM.

CONCLUSIONS Results of the present study indicate that the proportion of patients with T1DM meeting the nutritional recommendations is low. Meeting the nutrition recommendations for T1DM is associated with some benefits, and examining individual nutrient intakes might be useful, yet examining the alignment of the diet with a global Mediterranean-style dietary pattern seems more informative. Alignment of the diet with a Mediterranean-style dietary pattern is associated with both the anthropometric and metabolic profiles. These results suggest potential benefits of a Mediterranean-style dietary pattern for adults with T1DM. Further research is needed to confirm these findings.

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RESEARCH AUTHOR INFORMATION V. Gingras is a doctoral student, C. Leroux and K. Desjardins are research assistants, V. Savard is a master’s student, R. Rabasa-Lhoret is an endocrinologist and full professor, and I. Strychar is a full professor and an invited researcher, Institut de Recherches Cliniques de Montréal, Department of Nutrition, University of Montreal, Québec, Canada. S. Lemieux is full professor, Institute of Nutrition and Functional Foods, Laval University, Québec City, Québec, Canada. Address correspondence to: Rémi Rabasa-Lhoret, MD, PhD, Department of Nutrition, Montreal University, Institut de Recherches Cliniques de Montréal (IRCM), 110 Ave des Pins Ouest, Montréal, Québec H2W 1R7, Canada. E-mail: [email protected]

STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.

FUNDING/SUPPORT This work represents secondary analysis of a cohort study funded by a grant from Diabète Québec, as well as the J. A. deSève chair. V. Gingras and R. Rabasa-Lhoret are research scholars of FRQ-S (Fonds de Recherche du Québec en Santé).

ACKNOWLEDGEMENTS The authors thank all the participants of this study. The authors would also like to express their gratitude to the endocrinologists from the Montreal University Hospital Centre endocrine division and the Diabète Québec organization for their help with the recruitment. The authors thank Hortensia Mircescu, MD, for her help with recruitment of participants and medical visits. Finally, the authors thank Maryse Lefebvre, RD, for her contribution to the analyses of the food records.

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